Yundan Wang, Xiwen Tong, Shenglei Yuan, Pengcheng Yang, Ling Li, Yong Zhao, and Le Kang

PNAS February 8, 2022 119 (6) e2120835119

Significance

Ecological immunology addresses the interactions between host immunity and the environment. Locusts display density-dependent phase transitions between solitary and gregarious locusts. In control practices and laboratory bioassays, gregarious locusts always exhibit stronger resistance to fungal pathogens than solitary locusts. However, few studies have investigated the mechanism of altered immune switch in locusts. Here, we combined mathematical simulation and experimental studies to show that gregarious locusts inhibit tumor necrosis factor (TNF) to alter immune defense by enhancing humoral defense and reducing cellular defense, and high levels of TNF reduce the survival of solitary locusts. Our study provides an important cue for understanding cellular immunity variations in response to different population densities and for improving the control efficacy of locust plagues.

Abstract

Changes in population density lead to phenotypic differentiation of solitary and gregarious locusts, which display different resistance to fungal pathogens; however, how to regulate their cellular immune strategies remains unknown. Here, our stochastic simulation of pathogen proliferation suggested that humoral defense always enhanced resistance to fungal pathogens, while phagocytosis sometimes reduced defense against pathogens. Further experimental data proved that gregarious locusts had significantly decreased phagocytosis of hemocytes compared to solitary locusts. Additionally, transcriptional analysis showed that gregarious locusts promoted immune effector expression (gnbp1 and dfp) and reduced phagocytic gene expression (eater) and the cytokine tumor necrosis factor (TNF). Interestingly, higher expression of the cytokine TNF in solitary locusts simultaneously promoted eater expression and inhibited gnbp1 and dfp expression. Moreover, inhibition of TNF increased the survival of solitary locusts, and injection of TNF decreased the survival of gregarious locusts after fungal infection. Therefore, our results indicate that the alerted expression of TNF regulated the immune strategy of locusts to adapt to environmental changes.

See: https://www.pnas.org/content/119/6/e2120835119

Fig. 1.

Stochastic simulation of hemocytes and pathogen growth in altered immune defenses. (A) The schematic of humoral and cellular defense in host resist pathogen infection. α indicates the increase rate of hemocytes for the total events of the proliferation, migration, and death, and β indicates the increase rate of microbes including the total events of the proliferation and death by humoral attack. K1, K2, and K3 indicates the rate of phagocytosis efficient, phagocytes recovery, and phagocytes death (microbe escape) respectively. (B) To observe the competence of hemocytes and microbe growth, various status of cellular defense, microbe virulence and humoral defenses were examined in simulation. All status (8 combinations) of cellular defense, humoral defense, and microbe virulence (high or low) were observed in the simulation. (C) Kinetic curves of hemocytes and microbes by immune defense of high humoral and high cellular defenses. Left indicates status 3 and Right indicates status 4. (D) Kinetic curves of hemocytes and microbes by immune defense of high humoral and low cellular defenses. Left indicates status 6 and Right indicates status 8.